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Biomineralization Forming Process and Bio-Inspired Nanomaterials for Biomedical Application: a Review

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Review Biomineralization Forming Process and Bio-inspired Nanomaterials for Biomedical Application: A Review Yuanyuan Chen 1,2, Yanmin Feng 1,2,*, John Gregory Deveaux 1, Mohamed Ahmed Masoud 1, Felix Sunata Chandra 1, Huawei Chen 1,2, Deyuan Zhang 1,2 and Lin Feng 1,2,* 1 School of Mechanical Engineering & Automation, Beihang University, Beijing 100191, China; [email protected] (Y.C.); [email protected] (J.G.D.); [email protected] (M.A.M.); [email protected] (F.S.C.); [email protected] (H.C.); [email protected] (D.Z.) 2 Beijing Advanced Innovation Center for Biomedical Engineering, Beihang University, Beijing 100083, China * Correspondence: [email protected] (Y.F.); [email protected] (L.F.) Received: 20 December 2018; Accepted: 17 January 2019; Published: 23 January 2019 Abstract: Biomineralization is a process in which organic matter and inorganic matter combine with each other under the regulation of living organisms. Because of the biomineralization-induced super survivability and retentivity, biomineralization has attracted special attention from biologists, archaeologists, chemists, and materials scientists for its tracer and transformation effect in rock evolution study and nanomaterials synthesis. However, controlling the biomineralization process in vitro as precisely as intricate biology systems still remains a challenge. In this review, the regulating roles of temperature, pH, and organics in biominerals forming process were reviewed. The artificially introducing and utilization of biomineralization, the bio-inspired synthesis of nanomaterials, in biomedical fields was further discussed, mainly in five potential fields: drug and cell-therapy engineering, cancer/tumor target engineering, bone tissue engineering, and other advanced biomedical engineering. This review might help other interdisciplinary researchers to bionic-manufacture biominerals in molecular-level for developing more applications of biomineralization. Keywords: biomineralization; biological control; biomimetic mineralization; nanomaterial; biomedical engineering 1. Introduction As a natural protective structure, biomineralization is a process in which organic matter and inorganic matter combine with each other under the regulation of living organisms [1]. Biomineralized crystals are different from the regular structure and surface of artificial crystals. According to the growing environment, biomineralized crystals exhibit distinct physical and chemical characteristics, which are difficult to simulate and manufacture in vitro, while the biomineralization forming process is much similar. As the development of image representation technology, the biomineralization forming mechanism has been found and defined, and their classification has been discussed in some review papers from different systems [2–4]. Based on this, many bio-inspired nanomaterials were created through simulating or mimicking the biomineralization forming process. Biomineralization is a widespread phenomenon that leads to the formation of well-organized biominerals，which refers to the formation of inorganic minerals in organisms [3]. These inorganic minerals not only help to protect the living organisms, like mature mollusk shells [5], brachiopod shells [6], and crustacean cuticles [7], but also help to support organisms and sense signals from surroundings, like bones [8], teeth [9], echinoderm skeletons [10], coral skeleton [11,12], and sponge spicules [13]. C.J.G., et al. [14] have described the mechanism, structure, and bio-function of Minerals 2019, 9, 68; doi:10.3390/min9020068 www.mdpi.com/journal/minerals Minerals 2019, 9, 68 2 of 21 skeleton-shaped biomineralization in detail in a book. Biomineralization involves biology, chemistry, crystallography, materials science, mineralogy, and medicine, and other disciplines have also led to specialization in these fields. Studying the characteristics of biomineralization forming mechanism is not only helpful to the development and utilization of new nanomaterials, but also helps to treat abnormal mineralization that is caused by the human body disease, such as osteoporosis, osteomalacia, hypophosphatasia, kidney stones, and atherosclerosis. On the other hand, various nano-functional materials were synthesized and biomineralized with living characteristics. Because of the biomineralization-induced super survivability and retentivity, biomineralization has attracted special attention from biologists, archaeologists, chemists, and materials scientists for its tracer and transformation effect in rock evolution study and nanomaterials synthesis. However, controlling the biomineralization process in vitro as precisely as intricate biology systems still remains a challenge. In this report, we first reviewed the biomineralization forming process in Section 2, including the general crystal growth type, the factors affecting biomineral formation, mechanism and approach of mineralization, and biomimetic biomineralization. In Section 3, the latest applications of biomineralization in biomedical engineering were summarized. Also, Section 4 discussed the future perspectives of biomineralization. This review might help other interdisciplinary researchers to simulate, and bionic-manufacture biominerals in molecular-level for developing more applications for biomineralization. 2. Biomineralization Forming Process 2.1. The Type of Mineralization According to the degree of biological mineral control, biomineralization could be divided into two categories: biological induction and biological control. Bio-induced biomineralization is a process caused by physiological activities of organisms, such as metabolism, inhalation of oxygen, exhalation of carbon dioxide by respiration, as well as establishment of cell walls, which change the physical and chemical conditions of the surrounding environments. This mineralization is not guided by specific cell tissues or biological macromolecules, resulting in arbitrary orientation of crystals and lack of unique morphology. Negatively charged cell walls (containing carboxyl and phosphatidyl groups) combine Fe3+ ions by electrostatic interaction, and Fe3+ ions react with silicic acid to form iron silicate. This process is seldom controlled by cells, and its crystalline form is similar to that of iron silicate that is produced in inorganic solutions. Biologically controlled mineralization is a process that is caused by biological physiological activities and controlled by biology in three aspects: space, structure, and chemistry. It occurs in delineated confined spaces. Biomineral organic matter is formed with high content, unique crystallization habit, uniform size, uniform shape, and regular arrangement. There are two forms of mineralization: one is normal mineralization, such as skeleton, teeth and shellfish, formation of shells, and so on. Another is abnormal mineralization, such as stones, dental stones and caries teeth, and so on. There are two theories to explain this biomineralization. Solution crystallization theory and polymer-induced liquid phase precursor mineralization theory. For solution crystallization theory, Type I collagen molecules self-assemble into a native “hole”, the “hole” contain negatively charged amino acids, the –COO– could bind to Ca2+, which lead to the deposition of Ca2+ in the “hole”[15]. After deposition, the calcium phosphate (Ca-Pi) is electrostatically formed through binding. The Ca–Pi nucleus is the basic building blocks of bone structure [16]. In addition, the “hole” is the nucleation site of hydroxyapatite crystals, which is another important component of bones [17]. For polymer-induced liquid phase precursor mineralization theory, highly hydrated amorphous calcium phosphate phase nanometer droplets penetrate into the pores and voids of collagen fibers the hydrates lose water and crystallize in the pores and voids of collagen fibers [18]. The calcification of atherosclerosis (AS) plaque is a typical sample of abnormal mineralization. Minerals 2019, 9, 68 3 of 21 2.2. Factors Controlling Biomineralization Mineralization in organisms can be divided into four stages. (1) Organic macromolecules are pre-assembled into ordered structures. Insoluble organic matter in organisms constructs an organized micro-reaction environment before mineral deposition, which determines the location of inorganic nucleation and the function of mineral formation. This stage is the precondition of biomineralization. (2) Molecular recognition of organic-inorganic interfaces controlling crystal nucleation and growth. (3) Growth regulation enabling the initial assembly of crystals to form subunits. (4) Cell prepressing, forming biominerals with multilevel structure by assembling subunit minerals. It is believed that biomineralization is controlled by varying factors. The formation of biominerals is often the result of the synergistic action of various factors, including pH, temperature, and matrix. 2.2.1. Temperature and pH Temperature is an important factor affecting calcium carbonate deposition. The solubility of most salts in water will increase with the increase of temperature. However, calcium carbonate has abnormal solubility, the solubility will decrease when the temperature rises. That is to say, more calcium carbonate will deposit when the temperature rise. pH also has great influence on the solubility of carbonate. Reducing PH value will increase the solubility of carbonate. Furthermore, pH and temperatures can control calcium carbonate particles forming
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